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The Role of Alternative Prey in Sustaining Predator Populations

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The Role of Alternative Prey in Sustaining Predator Populations ___________________________________ The Role of Alternative Prey in Sustaining Predator Populations THE ROLE OF ALTERNATIVE PREY IN SUSTAINING PREDATOR POPULATIONS James D. HARWOOD and John J. OBRYCKI Department of Entomology, University of Kentucky S-225 Agricultural Science Center North Lexington, Kentucky 40546-0091 U.S.A. [email protected] [email protected] ABSTRACT Generalist predators are widely acknowledged to contribute valuable levels of biological con- trol in agroecosystems throughout the world. Although their feeding habits can result in the rejection of target pests in favor of preferred and often more nutritious non-pest prey, these natural enemies are capable of colonizing habitats prior to the arrival of pests by subsisting on alternative sources of food. The effect of consuming non-pest species on rates of pest preda- tion by a generalist predator can be twofold; feeding upon these nutritious food items gener- ally enhances fecundity thus improving their population growth, but the presence of alterna- 453 tive prey, especially during times when pest regulation is required, can result in reduced levels of pest consumption per individual predator. However, an increased density of natural en- emies can counteract this reduction in pest consumption and exert significant levels of bio- logical control. The role of alternative prey in sustaining predator populations has been widely reported in laboratory studies and field trials examining the fecundity, feeding behavior and growth rates of species subjected to diets of varying quality. Recently, the application of monoclonal antibody and molecular technology to study predation rates in the field has revealed the ex- tent to which many predator communities rely on alternative prey before, during and after the immigration of pests into crops. In this study we examine the role of key species of alter- native prey to generalist predators and discuss their impact in the context of biological con- trol. The importance of these prey items to sustaining linyphiid spider and coccinellid com- munities will also be examined. Microsite sampling of arthropod populations in alfalfa indi- cated that the overlap in availability of pests (Acyrthosiphon pisum and Empoasca fabae) and alternative prey to linyphiid spiders is likely to reduce the ability of these generalist predators to restrict the growth of pest populations. INTRODUCTION Generalist predators, as part of a complex community of natural enemies, can make signifi- cant contributions to the biological control of many pests (Obrycki and Kring 1998; Sunderland et al. 1997; Symondson et al., 2002). Although they readily consume target pests, their polypha- Second International Symposium on Biological Control of Arthropods Harwood and Obrycki _________________________________________________________________________ gous feeding habits can result in alternative non-pest food resources constituting a significant component of their diet. Furthermore, the availability of these alternative food items can affect pest consumption rates in the field (Harper et al. 2005; Harwood et al. 2004) and reduce their role in integrated pest management. Despite this interference, these arthropods are ca- pable of impacting upon pests once they arrive in the crop, employing a “lying-in-wait” strat- egy by subsisting on alternative prey (Chang and Kareiva 1999; Murdoch et al. 1985) and impacting upon pests with favorable predator:pest ratios when control is required (Settle et al. 1996). However, many species of alternative prey are preferred food items (Toft 2005) and increase growth rates (Mayntz and Toft 2001; Toft 1995), while pests may even elicit aver- sions from some predators after extended exposure (Toft 1997). This diversion away from target pests thus reduces their capacity for effective biological control (Koss and Snyder 2005; Koss et al. 2004; Madsen et al. 2004) (Fig. 1). However, simply because pests are a poor quality prey item (Toft 2005) does not necessarily translate to little or no biological control in the field where generalist predators are frequently in a state of hunger (e.g., Bilde and Toft 1998) and readily consume these prey (Harwood et al. 2004; 2005). Increased consumption of Increased pests by predator Biocontrol population Rapid increase in generalist predator High density of alternative population through increase 454 prey reproduction and immigration Reduced pest consumption due to preferential Reduced predation on Biocontrol alternative prey Predator population Limited pest Low density Reduction remains low consumption of alternative and delay of and due to small prey biological emigration predator control rates high population Figure 1. The role of alternative prey in mechanisms of biological control by generalist predator populations. Many predators build up their populations early in the season by feeding on alternative prey items which are abundant at this time of year (Harwood et al. 2001; 2003). This enables them to impact upon pests as soon as they arrive and has been supported by the mathematical modeling of pest populations (Fleming 1980). Murdoch et al. (1985) even suggested that gen- eralist predators could be more valuable in biological control than individual specialists act- ing alone. Early season predation could be extremely important in the control of pests such as the potato leafhopper, Empoasca fabae (Harris) (Homoptera: Cicadellidae), since control measures are generally required before injury symptoms first appear (Steffey and Armbrust Second International Symposium on Biological Control of Arthropods ___________________________________ The Role of Alternative Prey in Sustaining Predator Populations 1991). The presence of a “lying in wait” predator complex could therefore restrict population growth when their densities are low and before specialist natural enemies colonize the habi- tat. This study examines the role of alternative sources of food in sustaining populations of two different groups of predator: spiders (true generalists) and coccinellids (aphidophagous predators that exhibit some generalist habits). Field research will focus on the importance of alternative prey to the diet of linyphiid spiders in alfalfa and form a baseline of ecological data for the subsequent molecular analysis of predator feeding habits in the field. MATERIALS AND METHODS Adult coccinellids, Harmonia axyridis (Pallas) (Coleoptera: Coccinellidae), and spiders, Erigone autumnalis (Emerton) (Araneae: Linyphiidae), were collected from the University of Ken- tucky Spindletop Research Station and maintained in the laboratory at 21°C on a 16:8 L:D cycle. Prior to laboratory experiments (below), all individuals were provided with an ad libi- tum supply of isotomid Collembola and Diptera (for spiders) or aphids (for coccinellids). EFFECTS OF ALTERNATIVE PREY ON HARMONIA AXYRIDIS Adult male and female H. axyridis were paired and provided an ad libitum diet of Acyrthosiphon pisum (Harris) (Hemiptera: Aphididae) and Drosophila melanogaster Meigen (Diptera: Drosophilidae) larvae. Eggs were collected, maintained at 21°C on a 16:8 L:D cycle, and upon hatching equal numbers of larvae were systematically assigned to one of five treatments (Table 455 1). Three parameters were measured; (a) percentage survival to adult, (b) mean development time, and (c) mean weight of adult females at emergence. Table 1. Invertebrate prey added to each of five treatments. Food was supplied ad libitum to all coccinellid larvae. Treatment Prey species A Danaus plexippus (L.) (Lepidoptera: Nymphalidae) B Papilio polyxenes F. (Lepidoptera: Papilionidae) CMixed diet of Danaus plexippus and Papilio polyxenes D Aphis glycines Matsumura (Hemiptera: Aphididae) E Aphis glycines, Danaus plexippus and Papilio polyxenes EFFECTS OF ALTERNATIVE PREY ON ERIGONE AUTUMNALIS Adult male and female E. autumnalis were paired and provided with an ad libitum diet of alternative and pest prey (Table 2). Eggsacs were collected and upon hatching, spiderlings were separated and placed into individual Petri dishes with a moist Plaster-of-Paris base to maintain high humidity. Equal numbers of individuals were systematically assigned to one of six treatments (Table 2) after the first molt. Prior to this, small isotomid and sminthurid Second International Symposium on Biological Control of Arthropods Harwood and Obrycki _________________________________________________________________________ Table 2. Invertebrate prey added to each of six treatments. Food was supplied ad libitum to all spiderlings. Treatment Prey species A Isotomid Collembola B Drosophila melanogaster C Acyrthosiphon pisum D Empoasca fabae E Acyrthosiphon pisum and Empoasca fabae F Mixed diet of Isotomid Collembola, Drosophila melanogaster, Acyrthosiphon pisum and Empoasca fabae Collembola were provided as prey (large food items were not taken by first instar linyphiid spiderlings). Three parameters were measured; (a) percentage survival to adult, (b) mean de- velopment time, and (c) mean weight of new adult females. INTERACTIONS BETWEEN ALTERNATIVE PREY AND PESTS IN ALFALFA Quantifying the availability of pest and non-pest prey to linyphiid spiders was undertaken in alfalfa fields at the University of Kentucky Spindletop Research Station. Linyphiid spiders 456 were collected weekly from May until August and immediately frozen in separate Eppendorf tubes (for subsequent molecular analysis of gut-content). The availability of prey was moni- tored by mini-sticky traps following protocols described
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